Analysis of Three-Dimensional Cell Migration in Dopamine-Modified Poly(aspartic acid)-Based Hydrogels
Abstract
:1. Introduction
2. Results and Discussion
2.1. Characterization of PSI, PASP Based Polymers, and PASP-Based Hydrogels
2.2. Dopamine Release during the Hydrolysis of the Gels
2.3. Cell Viability and Morphology on Different PASP-DA Hydrogels
2.4. Three-Dimensional Distribution of PDLCs and SH-SY5Y Cells on PASP-DA Hydrogels
3. Conclusions
4. Materials and Methods
4.1. Preparation of Dopamine Modified Poly(succinimide)s
4.2. Chemical Characterization by Nuclear Magnetic Resonance (NMR) Spectroscopy
4.3. Preparation and Characterization of DA Containing PASP-Based Hydrogels
4.4. Determination of the DA Content of the PASP Hydrogels
4.5. Culturing of PDLCs and SH-SY5Y Cells
4.6. Cell Viability Assay
4.7. Cell Morphological Studies
4.8. Analysis of the Two-Photon Microscopic Images
4.9. Statistical Analysis
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Berthiaume, F.; Maguire, T.J.; Yarmush, M.L. Tissue Engineering and Regenerative Medicine: History, Progress, and Challenges. Annu. Rev. Chem. Biomol. Eng. 2011, 2, 403–430. [Google Scholar] [CrossRef] [PubMed]
- Wobma, H.; Vunjak-Novakovic, G. Tissue Engineering and Regenerative Medicine 2015: A Year in Review. Tissue Eng. Part B Rev. 2016, 22, 101–113. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bajaj, P.; Schweller, R.M.; Khademhosseini, A.; West, J.L.; Bashir, R. 3D Biofabrication Strategies for Tissue Engineering and Regenerative Medicine. Annu. Rev. Biomed. Eng. 2014, 16, 247–276. [Google Scholar] [CrossRef] [Green Version]
- Abdelfattah, M.I.; Nasry, S.A.; Mostafa, A.A. Characterization and Cytotoxicity Analysis of a Ciprofloxacin Loaded Chitosan/Bioglass Scaffold on Cultured Human Periodontal Ligament Stem Cells: A Preliminary Report. Maced. J. Med. Sci. 2016, 4, 461–467. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Drury, J.L.; Mooney, D.J. Hydrogels for Tissue Engineering: Scaffold Design Variables and Applications. Biomaterials 2003, 24, 4337–4351. [Google Scholar] [CrossRef]
- Ling-Ling, E.; Xu, W.H.; Feng, L.; Liu, Y.; Cai, D.Q.; Wen, N.; Zheng, W.J. Estrogen Enhances the Bone Regeneration Potential of Periodontal Ligament Stem Cells Derived from Osteoporotic Rats and Seeded on Nano-Hydroxyapatite/Collagen/Poly(L-Lactide). Int. J. Mol. Med. 2016, 37, 1475–1486. [Google Scholar] [CrossRef] [Green Version]
- Jo, B.S.; Lee, Y.; Suh, J.S.; Park, Y.S.; Lee, H.J.; Cho, J.; Lee, G.; Chung, C.P.; Park, K.D.; Jeong, Y. A Novel Calcium-Accumulating Peptide/Gelatin in Situ Forming Hydrogel for Enhanced Bone Regeneration. J. Biomed. Mater. Res. 2018, 106, 1–30. [Google Scholar] [CrossRef] [PubMed]
- Juriga, D.; Nagy, K.; Jedlovszky-Hajdú, A.; Perczel-Kovách, K.; Chen, Y.M.; Varga, G.; Zrínyi, M. Biodegradation and Osteosarcoma Cell Cultivation on Poly(Aspartic Acid) Based Hydrogels. ACS Appl. Mater. Interfaces 2016, 8, 23463–23476. [Google Scholar] [CrossRef]
- Discher, D.E.; Mooney, D.J.; Zandstra, P.W. Growth Factors, Matrices, and Forces Combine and Control Stem Cells. Science 2009, 324, 1673–1677. [Google Scholar] [CrossRef] [Green Version]
- Svobodová, J.; Proks, V.; Karabiyik, Ö.; Koyuncu, A.C.C.; Köse, G.T.; Rypáček, F.; Studenovská, H. Poly(Amino Acid)-Based Fibrous Scaffolds Modified with Surface-Pendant Peptides for Cartilage Tissue Engineering. J. Tissue Eng. Regen. Med. 2017, 11, 831–842. [Google Scholar] [CrossRef]
- Adelnia, H.; Tran, H.D.N.; Little, P.J.; Blakey, I.; Ta, H.T. Poly(Aspartic Acid) in Biomedical Applications: From Polymerization, Modification, Properties, Degradation, and Biocompatibility to Applications. ACS Biomater. Sci. Eng. 2021, 7, 2083–2105. [Google Scholar] [CrossRef]
- Zrinyi, M.; Gyenes, T.; Juriga, D.; Kim, J. Acta Biomaterialia Volume Change of Double Cross-Linked Poly(Aspartic Acid) Hydrogels Induced by Cleavage of One of the Crosslinks Thermal Treatment. Acta Biomater. 2013, 9, 5122–5131. [Google Scholar] [CrossRef]
- Molnar, K.; Juriga, D.; Nagy, P.M.; Sinko, K.; Jedlovszky-Hajdu, A.; Zrinyi, M. Electrospun Poly(Aspartic Acid) Gel Scaffolds for Artificial Extracellular Matrix. Polym. Int. 2014, 63, 1608–1615. [Google Scholar] [CrossRef]
- Juriga, D.; Sipos, E.; Heged, O.; Varga, G.; Zrínyi, M.; Nagy, K.S.; Jedlovszky-hajdú, A. Fully Amino Acid-Based Hydrogel as Potential Scaffold for Cell Culturing and Drug Delivery. Beilstein J. Nanotechnol. 2019, 10, 2579–2593. [Google Scholar] [CrossRef] [PubMed]
- Hegedus, O.; Juriga, D.; Sipos, E.; Voniatis, C.; Juhász, Á.; Idrissi, A.; Zrínyi, M.; Varga, G.; Jedlovszky-Hajdú, A.; Nagy, K.S. Free Thiol Groups on Poly(Aspartamide) Based Hydrogels Facilitate Tooth-Derived Progenitor Cell Proliferation and Differentiation. PLoS ONE 2019, 14, e0226363. [Google Scholar] [CrossRef] [PubMed]
- Németh, C.; Gyarmati, B.; Abdullin, T.; László, K.; Szilágyi, A. Poly(Aspartic Acid) with Adjustable PH-Dependent Solubility. Acta Biomater. 2017, 49, 486–494. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Németh, C.; Szabó, D.; Gyarmati, B.; Gerasimov, A.; Varfolomeev, M.; Abdullin, T.; László, K.; Szilágyi, A. Effect of Side Groups on the Properties of Cationic Polyaspartamides. Eur. Polym. J. 2017, 93, 805–814. [Google Scholar] [CrossRef] [Green Version]
- Juriga, D.; Laszlo, I.; Ludanyi, K.; Klebovich, I.; Chae, C.H.; Zrinyi, M. Kinetics of Dopamine Release from Poly(Aspartamide)-Based Prodrugs. Acta Biomater. 2018, 76, 225–238. [Google Scholar] [CrossRef] [PubMed]
- Foley, P.B. Dopamine in Psychiatry: A Historical Perspective. J. Neural Transm. 2019, 126, 473–479. [Google Scholar] [CrossRef] [PubMed]
- Papalini, S.; Beckers, T.; Vervliet, B. Dopamine: From Prediction Error to Psychotherapy. Transl. Psychiatry 2020, 10, 164. [Google Scholar] [CrossRef]
- Lee, J.S.; Yi, J.K.; An, S.Y.; Heo, J.S. Increased Osteogenic Differentiation of Periodontal Ligament Stem Cells on Polydopamine Film Occurs via Activation of Integrin and PI3K Signaling Pathways. Cell. Physiol. Biochem. 2014, 34, 1824–1834. [Google Scholar] [CrossRef] [PubMed]
- Han, L.; Lu, X.; Liu, K.; Wang, K.; Fang, L.; Weng, L.T.; Zhang, H.; Tang, Y.; Ren, F.; Zhao, C.; et al. Mussel-Inspired Adhesive and Tough Hydrogel Based on Nanoclay Confined Dopamine Polymerization. ACS Nano 2017, 11, 2561–2574. [Google Scholar] [CrossRef]
- Cencer, M.; Liu, Y.; Winter, A.; Murley, M.; Meng, H.; Lee, B.P. Effect of PH on the Rate of Curing and Bioadhesive Properties of Dopamine Functionalized Poly(Ethylene Glycol) Hydrogels. Biomacromolecules 2014, 15, 2861–2869. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cui, J.; Iturri, J.; Paez, J.; Shafiq, Z.; Serrano, C.; d’Ischia, M.; del Campo, A.; Shafi, Z.; Serrano, C.; Ischia, M.; et al. Dopamine-Based Coatings and Hydrogels: Toward Substitution-Related Structure–Property Relationships. Macromol. Chem. Phys. 2014, 215, 2403–2413. [Google Scholar] [CrossRef]
- Scognamiglio, F.; Travan, A.; Borgogna, M.; Donati, I.; Marsich, E.; Bosmans, J.W.A.M.; Perge, L.; Foulc, M.P.; Bouvy, N.D.; Paoletti, S. Enhanced Bioadhesivity of Dopamine-Functionalized Polysaccharidic Membranes for General Surgery Applications. Acta Biomater. 2016, 44, 232–242. [Google Scholar] [CrossRef] [PubMed]
- Baudry, A.; Alleaume-Butaux, A.; Dimitrova-Nakov, S.; Goldberg, M.; Schneider, B.; Launay, J.M.; Kellermann, O. Essential Roles of Dopamine and Serotonin in Tooth Repair: Functional Interplay between Odontogenic Stem Cells and Platelets. Stem Cells 2015, 33, 2586–2595. [Google Scholar] [CrossRef]
- Wang, W.; Zhao, L.; Bai, F.; Zhang, T.; Dong, H.; Liu, L. The Protective Effect of Dopamine against OGD/R Injury-Induced Cell Death in HT22 Mouse Hippocampal Cells. Environ. Toxicol. Pharmacol. 2016, 42, 176–182. [Google Scholar] [CrossRef]
- Varella, M.H.; De Mello, F.G.; Linden, R. Evidence for an Antiapoptotic Role of Dopamine in Developing Retinal Tissue. J. Neurochem. 1999, 73, 485–492. [Google Scholar] [CrossRef]
- Bozzi, Y.; Borrelli, E. Dopamine in Neurotoxicity and Neuroprotection: What Do D2 Receptors Have to Do with It? Trends Neurosci. 2006, 29, 167–174. [Google Scholar] [CrossRef]
- Seo, B.; Miura, M.; Gronthos, S.; Bartold, P.M.; Batouli, S.; Brahim, J.; Young, M.; Robey, P.G.; Wang, C.; Shi, S. Investigation of Multipotent Postnatal Stem Cells from Human Periodontal Ligament. Natl. Libr. Med. 2004, 369, 149–155. [Google Scholar] [CrossRef]
- Ivanovski, S.; Gronthos, S.; Shi, S.; Bartold, P.M. Stem Cells in the Periodontal Ligament. Oral Dis. 2006, 12, 358–363. [Google Scholar] [CrossRef] [PubMed]
- Gay, I.C.; Chen, S.; MacDougall, M. Isolation and Characterization of Multipotent Human Periodontal Ligament Stem Cells. Orthod. Craniofac. Res. 2007, 10, 149–160. [Google Scholar] [CrossRef] [PubMed]
- Gronthos, S.; Mankani, M.; Brahim, J.; Robey, P.G.; Shi, S. Postnatal Human Dental Pulp Stem Cells (DPSCs) in Vitro and in Vivo. Proc. Natl. Acad. Sci. USA 2000, 97, 13625–13630. [Google Scholar] [CrossRef] [Green Version]
- Zhen, L.; Liu, H. Differentiation of Human Periodontal Ligament Stem Cells into Neuron-like Cells in Vitro. West China J. Stomatol. 2009, 27, 71–74. [Google Scholar]
- Menicanin, D.; Mrozik, K.M.; Wada, N.; Marino, V.; Shi, S.; Bartold, P.M.; Gronthos, S. Periodontal-Ligament-Derived Stem Cells Exhibit the Capacity for Long-Term Survival, Self-Renewal, and Regeneration of Multiple Tissue Types in Vivo. Stem Cells Dev. 2014, 23, 1001–1011. [Google Scholar] [CrossRef]
- Ansari, S.; Diniz, I.M.; Chen, C.; Sarrion, P.; Tamayol, A.; Wu, B.M.; Moshaverinia, A. Human Periodontal Ligament- and Gingiva-Derived Mesenchymal Stem Cells Promote Nerve Regeneration When Encapsulated in Alginate/Hyaluronic Acid 3D Scaffold. Adv. Healthc. Mater. 2017, 6, 1–10. [Google Scholar] [CrossRef]
- Moshaverinia, A.; Xu, X.; Chen, C.; Ansari, S.; Zadeh, H.H.; Snead, M.L.; Shi, S. Application of Stem Cells Derived from the Periodontal Ligament Orgingival Tissue Sources for Tendon Tissue Regeneration. Biomaterials 2014, 35, 2642–2650. [Google Scholar] [CrossRef] [Green Version]
- Fraser, D.; Nguyen, T.; Benoit, D.S.W. Matrix Control of Periodontal Ligament Cell Activity Via Synthetic Hydrogel Scaffolds. Tissue Eng. Part A 2021, 27, 733–747. [Google Scholar] [CrossRef] [PubMed]
- Kovalevich, J.; Langford, D. Considerations for the Use of SH-SY5Y Neuroblastoma Cells in Neurobiology. Methods Mol. Biol. 2013, 1078, 9–21. [Google Scholar] [CrossRef] [Green Version]
- Xicoy, H.; Wieringa, B.; Martens, G.J.M. The SH-SY5Y Cell Line in Parkinson’s Disease Research: A Systematic Review. Mol. Neurodegener. 2017, 12, 10. [Google Scholar] [CrossRef] [Green Version]
- Desai, A.; Kisaalita, W.S.; Keith, C.; Wu, Z.Z. Human Neuroblastoma (SH-SY5Y) Cell Culture and Differentiation in 3-D Collagen Hydrogels for Cell-Based Biosensing. Biosens. Bioelectron. 2006, 21, 1483–1492. [Google Scholar] [CrossRef] [PubMed]
- Innala, M.; Riebe, I.; Kuzmenko, V.; Sundberg, J.; Gatenholm, P.; Hanse, E.; Johannesson, S. 3D Culturing and Differentiation of SH-SY5Y Neuroblastoma Cells on Bacterial Nanocellulose Scaffolds. Artif. Cells Nanomed. Biotechnol. 2014, 42, 302–308. [Google Scholar] [CrossRef]
- Lin, C.H.; Nicol, C.J.B.; Cheng, Y.C.; Yen, C.; Wang, Y.S.; Chiang, M.C. Neuroprotective Effects of Resveratrol against Oxygen Glucose Deprivation Induced Mitochondrial Dysfunction by Activation of AMPK in SH-SY5Y Cells with 3D Gelatin Scaffold. Brain Res. 2020, 1726, 146492. [Google Scholar] [CrossRef]
- Gyarmati, B.; Krisch, E.; Szilágyi, A. In Situ Oxidation-Induced Gelation of Poly(Aspartic Acid) Thiomers. React. Funct. Polym. 2014, 84, 29–36. [Google Scholar] [CrossRef]
- Szilágyi, B.Á.; Gyarmati, B.; Horvát, G.; Laki, Á.; Budai-Szűcs, M.; Csányi, E.; Sandri, G.; Bonferoni, M.C.; Szilágyi, A. The Effect of Thiol Content on the Gelation and Mucoadhesion of Thiolated Poly(Aspartic Acid). Polym. Int. 2017, 66, 1538–1545. [Google Scholar] [CrossRef]
- Kim, H.Y.; Kim, N.H.; Lee, S.J.; Song, J.E.; Kwon, S.Y.; Wha, C.J.; Dongwon, L.; Khang, G. Effect of Pore Sizes of PLGA Scaffolds on Mechanical Properties and Cell Behaviour for Nucleus Pulposus Regeneration in Vivo. Pediatr. Endocrinol. Rev. 2015, 13, 512–520. [Google Scholar] [CrossRef]
- Flory, P.J. Principles of Polymer Chemistry, 1st ed.; Flory, P.J., Ed.; Cornell University Press: Ithaca, NY, USA, 1953. [Google Scholar]
- Horkay, F.; Hecht, A.-M.; Geissler, E. Thermodynamic Interaction Parameters in Polymer Solutions and Gels. J. Polym. Sci. Part B Polym. Phys. 1995, 33, 1641–1646. [Google Scholar] [CrossRef]
- Koshimura, K.; Tanaka, J.; Murakami, Y.; Kato, Y. Effects of Dopamine and L-DOPA on Survival of PC12 Cells. J. Neurosci. Res. 2000, 62, 112–119. [Google Scholar] [CrossRef]
- Zhang, J.; Kravtsov, V.; Amarnath, V.; Picklo, M.J.; Graham, D.G.; Montine, T.J. Enhancement of Dopaminergic Neurotoxicity by the Mercapturate of Dopamine: Relevance to Parkinson’s Disease. J. Neurochem. 2000, 74, 970–978. [Google Scholar] [CrossRef] [PubMed]
- Armando, I.; Villar, V.A.M.; Jose, P.A. Dopamine and Renal Function and Blood Pressure Regulation. Compr. Physiol. 2011, 1, 1075–1117. [Google Scholar] [CrossRef]
- Ko, C.-C.; Wang, Z.; Chen, S.; Bai, B.; Lee, D.J.; Diachina, S.; Li, Y.; Wong, S.W.; Tseng, H.C. Dopaminergic Enhancement of Cellular Adhesion in Bone Marrow Derived Mesenchymal Stem Cells (MSCs). J. Stem Cell Res. Ther. 2017, 7, 395. [Google Scholar] [CrossRef] [Green Version]
- Wang, S.; Mou, Z.; Ma, Y.; Li, J.; Li, J.; Ji, X.; Wu, K.; Li, L.; Lu, W.; Zhou, T. Dopamine Enhances the Response of Sunitinib in the Treatment of Drug-Resistant Breast Cancer: Involvement of Eradicating Cancer Stem-like Cells. Biochem. Pharmacol. 2015, 95, 98–109. [Google Scholar] [CrossRef] [PubMed]
- Kadar, K.; Kiraly, M.; Porcsalmy, B.; Molnar, B.; Racz, G.Z.; Blazsek, J.; Kallo, K.; Szabo, E.L.; Gera, I.; Gerber, G.; et al. Differentiation Potential of Stem Cells from Human Dental Origin-Promise for Tissue Engineering. J. Physiol. Pharmacol. 2009, 60 (Suppl. 7), 167–175. [Google Scholar]
- Xie, H.R.; Hu, L.S.; Li, G.Y. SH-SY5Y Human Neuroblastoma Cell Line: In Vitro Cell Model of Dopaminergic Neurons in Parkinson’s Disease. Chin. Med. J. Engl. 2010, 123, 1086–1092. [Google Scholar] [CrossRef] [PubMed]
- Chen, Q.; Tian, X.; Fan, J.; Tong, H.; Ao, Q. An Interpenetrating Alginate/Gelatin Network for Three-Dimensional (3D) Cell Cultures and Organ Bioprinting. Molecules 2020, 25, 756. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Entekhabi, E.; Nazarpak, M.H.; Moztarzadeh, F.; Sadeghi, A. Design and Manufacture of Neural Tissue Engineering Scaffolds Using Hyaluronic Acid and Polycaprolactone Nanofibers with Controlled Porosity. Mater. Sci. Eng. C 2016, 69, 380–387. [Google Scholar] [CrossRef]
- Wang, X.; Gu, Z.; Jiang, B.; Li, L.; Yu, X. Surface Modification of Strontium-Doped Porous Bioactive Ceramic Scaffolds via Poly(DOPA) Coating and Immobilizing Silk Fibroin for Excellent Angiogenic and Osteogenic Properties. Biomater. Sci. 2016, 4, 678–688. [Google Scholar] [CrossRef]
- Liu, Y.; Meng, H.; Qian, Z.; Fan, N.; Choi, W.; Zhao, F.; Lee, B.P. A Moldable Nanocomposite Hydrogel Composed of a Mussel-Inspired Polymer and a Nanosilicate as a Fit-to-Shape Tissue Sealant. Angew. Chem.-Int. Ed. 2017, 56, 4224–4228. [Google Scholar] [CrossRef] [Green Version]
- Liu, Y.; Meng, H.; Konst, S.; Sarmiento, R.; Rajachar, R.; Lee, B.P. Injectable Dopamine-Modified Poly(Ethylene Glycol) Nanocomposite Hydrogel with Enhanced Adhesive Property and Bioactivity. ACS Appl. Mater. Interfaces 2014, 6, 16982–16992. [Google Scholar] [CrossRef]
- Akcay, G.; Luttge, R. Stiff-to-Soft Transition from Glass to 3d Hydrogel Substrates in Neuronal Cell Culture. Micromachines 2021, 12, 165. [Google Scholar] [CrossRef]
- Gowda, A.H.J.; Bu, Y.; Kudina, O.; Krishna, K.V.; Bohara, R.A.; Eglin, D.; Pandit, A. Design of Tunable Gelatin-Dopamine Based Bioadhesives. Int. J. Biol. Macromol. 2020, 164, 1384–1391. [Google Scholar] [CrossRef]
- Gong, C.; Lu, C.; Li, B.; Shan, M.; Wu, G. Injectable Dopamine-Modified Poly(α,β-Aspartic Acid) Nanocomposite Hydrogel as Bioadhesive Drug Delivery System Chu. J. Biomed. Mater. Res. Part A 2017, 105, 1000–1008. [Google Scholar] [CrossRef] [PubMed]
- Ellis-Behnke, R.; Jonas, J.B. Redefining Tissue Engineering for Nanomedicine in Ophthalmology. Acta Ophthalmol. 2011, 89, 108–114. [Google Scholar] [CrossRef]
- Hadden, W.J.; Young, J.L.; Holle, A.W.; McFetridge, M.L.; Kim, D.Y.; Wijesinghe, P.; Taylor-Weiner, H.; Wen, J.H.; Lee, A.R.; Bieback, K.; et al. Stem Cell Migration and Mechanotransduction on Linear Stiffness Gradient Hydrogels. Proc. Natl. Acad. Sci. USA 2017, 114, 5647–5652. [Google Scholar] [CrossRef] [Green Version]
- Yamada, K.M.; Sixt, M. Mechanisms of 3D Cell Migration. Nat. Rev. Mol. Cell Biol. 2019, 20, 738–752. [Google Scholar] [CrossRef] [PubMed]
- Dravid, A.; Raos, B.; Aqrawe, Z.; Parittotokkaporn, S.; O’Carroll, S.J.; Svirskis, D. A Macroscopic Diffusion-Based Gradient Generator to Establish Concentration Gradients of Soluble Molecules Within Hydrogel Scaffolds for Cell Culture. Front. Chem. 2019, 7, 638. [Google Scholar] [CrossRef]
- Stocco, E.; Barbon, S.; Lora, L.; Grandi, F.; Sartore, L.; Tiengo, C.; Petrelli, L.; Dalzoppo, D.; Parnigotto, P.P.; Macchi, V.; et al. Partially Oxidized Polyvinyl Alcohol Conduitfor Peripheral Nerve Regeneration. Sci. Rep. 2018, 8, 604. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kondaveeti, S.; Semeano, A.T.S.; Cornejo, D.R.; Ulrich, H.; Petri, D.F.S. Magnetic Hydrogels for Levodopa Release and Cell Stimulation Triggered by External Magnetic Field. Colloids Surf. B Biointerfaces 2018, 167, 415–424. [Google Scholar] [CrossRef]
- Santhosh, M.; Choi, J.H.; Choi, J.W. Magnetic-Assisted Cell Alignment within a Magnetic Nanoparticle-Decorated Reduced Graphene Oxide/Collagen 3D Nanocomposite Hydrogel. Nanomaterials 2019, 9, 1293. [Google Scholar] [CrossRef] [Green Version]
- Ashworth, J.C.; Mehr, M.; Buxton, P.G.; Best, S.M.; Cameron, R.E. Optimising Collagen Scaffold Architecture for Enhanced Periodontal Ligament Fibroblast Migration. J. Mater. Sci. Mater. Med. 2018, 29, 166. [Google Scholar] [CrossRef] [Green Version]
- Matsugami, D.; Murakami, T.; Yoshida, W.; Imamura, K.; Bizenjima, T.; Seshima, F.; Saito, A. Treatment with Functionalized Designer Self-Assembling Peptide Hydrogels Promotes Healing of Experimental Periodontal Defects. J. Periodontal Res. 2021, 56, 162–172. [Google Scholar] [CrossRef] [PubMed]
- Meiser, J.; Weindl, D.; Hiller, K. Complexity of Dopamine Metabolism. Cell Commun. Signal. 2013, 11, 1–18. [Google Scholar] [CrossRef] [Green Version]
- Hurd, T.R.; DeGennaro, M.; Lehmann, R. Redox Regulation of Cell Migration and Adhesion. Trends Cell Biol. 2012, 22, 107–115. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reczek, C.R.; Chandel, N.S. The Two Faces of Reactive Oxygen Species in Cancer. Annu. Rev. Cancer Biol. 2017, 1, 79–98. [Google Scholar] [CrossRef]
- Bórquez, D.A.; Urrutia, P.J.; Wilson, C.; Van Zundert, B.; Núñez, M.T.; González-Billault, C. Dissecting the Role of Redox Signaling in Neuronal Development. J. Neurochem. 2016, 137, 506–517. [Google Scholar] [CrossRef] [Green Version]
- Assis-de-Lemos, G.; Monteiro, J.; Oliveira-Valença, V.M.; Melo, G.A.; Reis, R.A.d.M.; Rehen, S.K.; Silveira, M.S.; Galina, A. Dopamine Signaling Impairs ROS Modulation by Mitochondrial Hexokinase in Human Neural Progenitor Cells. Biosci. Rep. 2021, 41, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Brenner-Lavie, H.; Klein, E.; Ben-Shachar, D. Mitochondrial Complex I as a Novel Target for Intraneuronal DA: Modulation of Respiration in Intact Cells. Biochem. Pharmacol. 2009, 78, 85–95. [Google Scholar] [CrossRef]
- Rana, D.; Colombani, T.; Mohammed, H.S.; Eggermont, L.J.; Johnson, S.; Annabi, N.; Bencherif, S.A. Strategies to Prevent Dopamine Oxidation and Related Cytotoxicity Using Various Antioxidants and Nitrogenation. Emergent Mater. 2019, 2, 209–217. [Google Scholar] [CrossRef]
- Jedlovszky-Hajdu, A.; Molnar, K.; Nagy, P.M.; Sinko, K.; Zrinyi, M. Preparation and Properties of a Magnetic Field Responsive Three-Dimensional Electrospun Polymer Scaffold. Colloids Surf. A Physicochem. Eng. Asp. 2016, 503, 79–87. [Google Scholar] [CrossRef] [Green Version]
- Nagy, K.; Láng, O.; Láng, J.; Perczel-Kovách, K.; Gyulai-Gaál, S.; Kádár, K.; Kőhidai, L.; Varga, G. A Novel Hydrogel Scaffold for Periodontal Ligament Stem Cells. Interv. Med. Appl. Sci. 2018, 10, 1–9. [Google Scholar] [CrossRef]
- Available online: http://citebay.com/how-to-cite/scikit-image/ (accessed on 1 December 2021).
- CitingSlicer. Available online: https://www.slicer.org/wiki/CitingSlicer (accessed on 1 December 2021).
DA0 | DA1/40 | DA1/20 | DA1/10 | |
---|---|---|---|---|
Average pore size | 120 ± 13 μm | 121 ± 25 μm | 110 ± 35 μm | 87 ± 27 μm |
Sample | Released Amount of DA (%) | DA Concentration in the Hydrogels after Hydrolysis (mmol/L) | Mass Swelling Degree |
---|---|---|---|
PASP-DA1/40 | 48.7 ± 4.81 | 4.73 ± 0.31 | 29.3 ± 0.6 |
PASP-DA1/20 | 58.3 ± 3.43 | 9.43 ± 0.78 | 21.8 ± 0.4 |
PASP-DA1/10 | 54.2 ± 3.44 | 23.96 ± 2.8 | 18.3 ± 0.3 |
Average Depth (μm) | ||
---|---|---|
PDLC | SH-SY5Y | |
Day 7 | 39 ± 18 | 24 ± 9 |
Day 14 | 75 ± 30 | 18 ± 8 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Juriga, D.; Kalman, E.E.; Toth, K.; Barczikai, D.; Szöllősi, D.; Földes, A.; Varga, G.; Zrinyi, M.; Jedlovszky-Hajdu, A.; Nagy, K.S. Analysis of Three-Dimensional Cell Migration in Dopamine-Modified Poly(aspartic acid)-Based Hydrogels. Gels 2022, 8, 65. https://doi.org/10.3390/gels8020065
Juriga D, Kalman EE, Toth K, Barczikai D, Szöllősi D, Földes A, Varga G, Zrinyi M, Jedlovszky-Hajdu A, Nagy KS. Analysis of Three-Dimensional Cell Migration in Dopamine-Modified Poly(aspartic acid)-Based Hydrogels. Gels. 2022; 8(2):65. https://doi.org/10.3390/gels8020065
Chicago/Turabian StyleJuriga, David, Eszter Eva Kalman, Krisztina Toth, Dora Barczikai, David Szöllősi, Anna Földes, Gabor Varga, Miklos Zrinyi, Angela Jedlovszky-Hajdu, and Krisztina S. Nagy. 2022. "Analysis of Three-Dimensional Cell Migration in Dopamine-Modified Poly(aspartic acid)-Based Hydrogels" Gels 8, no. 2: 65. https://doi.org/10.3390/gels8020065